Plant Ecology 151: 85–100, 2000. 85 © 2000 Kluwer Academic Publishers. Printed in the Netherlands. The evolution of vegetative desiccation tolerance in land plants Melvin J. Oliver1,Zoltan´ Tuba2 &BrentD.Mishler3 1Plant Stress and Water Conservation Laboratory, United States Department of Agriculture, Agricultural Research Service, Lubbock TX, USA (E-mail: [email protected]); 2Department of Botany and Plant Physiol- ogy, University of Agricultural Sciences, Gödöllõ, Hungary; 3University Herbarium, Jepson Herbarium, and Department of Integrative Biology, University of California, Berkeley, CA, USA Abstract Vegetative desiccation tolerance is a widespread but uncommon occurrence in the plant kingdom generally. The majority of vegetative desiccation-tolerant plants are found in the less complex clades that constitute the algae, lichens and bryophytes. However, within the larger and more complex groups of vascular land plants there are some 60 to 70 species of ferns and fern allies, and approximately 60 species of angiosperms that exhibit some degree of vegetative desiccation tolerance. In this report we analyze the evidence for the differing mechanisms of desiccation tolerance in different plants, including differences in cellular protection and cellular repair, and couple this evidence with a phylogenetic framework to generate a working hypothesis as to the evolution of desiccation tolerance in land plants. We hypothesize that the initial evolution of vegetative desiccation tolerance was a crucial step in the colonization of the land by primitive plants from an origin in fresh water. The primitive mechanism of tolerance probably involved constitutive cellular protection coupled with active cellular repair, similar to that described for modern-day desiccation-tolerant bryophytes. As plant species evolved, vegetative desiccation toler- ance was lost as increased growth rates, structural and morphological complexity, and mechanisms that conserve water within the plant and maintain efficient carbon fixation were selected for. Genes that had evolved for cellular protection and repair were, in all likelihood, recruited for different but related processes such as response to water stress and the desiccation tolerance of reproductive propagules. We thus hypothesize that the mechanism of desiccation tolerance exhibited in seeds, a developmentally induced cellular protection system, evolved from the primitive form of vegetative desiccation tolerance. Once established in seeds, this system became available for induction in vegetative tissues by environmental cues related to drying. The more recent, modified vegetative desiccation tolerance mechanism in angiosperms evolved from that programmed into seed development as species spread into very arid environments. Most recently, certain desiccation-tolerant monocots evolved the strategy of poikilochlorophylly to survive and compete in marginal habitats with variability in water availability. Introduction bryophytes. In a survey of the literature, Bewley & Krochko (1982) determined that within the larger and Desiccation tolerance, the ability to recover from the more complex groups of vascular land plants there almost complete loss (80–90%) of protoplasmic wa- are some 60 to 70 species of ferns and fern allies, ter, is a phenomenon common in the reproductive and approximately 60 species of angiosperms that ex- structures of green plants, pollen, spores and seeds. hibit some degree of vegetative desiccation tolerance However, the ability to survive desiccation in the vege- (Figures 1 and 2). The only major class of vascular tative stage is a widespread but uncommon occurrence plants that does not have a species that has desiccation- in the plant kingdom generally (Bewley & Krochko tolerant vegetative tissues is the gymnosperms (a tax- 1982; Oliver & Bewley 1997). The majority of vege- onomic group consisting of the phylogenetically dis- tative desiccation-tolerant plants are found in the less tinct cycads, conifers, and gnetophytes); Bewley & complex clades that constitute the algae, lichens and Krochko (1982) postulate that there may be a mini- 86 Figure 1. A phylogeny of the major groups of land plants, based on a consensus of several recent synthetic studies (Mishler & Churchill 1985; Crane 1990; Donoghue 1994; Mishler et al. 1994; Kenrick & Crane 1997), and information from workshops of the Green Plant Phylogeny Research Coordination Group. Names in bold and with an asterisk indicate clades with some known desiccation-tolerant members. Parsimony would suggest that while desiccation tolerance was primitive for the land plants, it was then lost early in the evolution of the tracheophytes, followed by at least one independent evolution (or re-evolution) of desiccation tolerance in Selaginella, in the ferns, and in the Angiosperms (see Figure 2 for a hypothesis of phylogenetic relationships within the Angiosperms). mum size limitation for desiccation tolerance, which are different in each of these lineages. This phyloge- members of this group exceed. netic evidence, combined with what we can deduce Recent synthetic phylogenetic analyses (summa- of the mechanisms by which plants achieve vegetative rized in Figures 1 and 2) suggest that vegetative desiccation tolerance, leads to a hypothesis as to the desiccation tolerance was primitively present in the nature and progression of the evolution of this trait. bryophytes (the basal-most living clades of land It is this hypothesis which serves as the focus of this plants), but was then lost in the evolution of tracheo- discourse. phytes. We postulate that the initial evolution of vege- Summarizing earlier studies, Bewley (1979) con- tative desiccation tolerance was a crucial step required cluded that there are three criteria which a plant or for the colonization of the land by primitive plants plant structure must meet in order to survive severe from a fresh water origin (Mishler & Churchill 1985), loss of protoplastic water. It must: (1) limit the dam- but that tolerance came at a cost, since metabolic age incurred to a repairable level, (2) maintain its rates in tolerant plants are low compared to those physiological integrity in the dried state (perhaps for in desiccation-sensitive plants. Thus, the loss of tol- extended periods of time), and (3) mobilize repair erance might have been favored along with the in- mechanisms upon rehydration which effect restitu- ternalization of water relationships that happened as tion of damage suffered during desiccation (and upon the vascular plants became more complex. However, the inrush of water back into the cells). Bewley & at least one independent evolution (or re-evolution) Oliver (1992) interpret these criteria to suggest that of desiccation tolerance occurred in Selaginella and desiccation tolerance can be achieved either by mech- again in the ferns. Within the angiosperms, at least anisms that are based on the protection of cellular eight independent cases of evolution (or re-evolution) integrity or mechanisms that are based on the repair of desiccation tolerance occurred. The natural rates of of desiccation- (or rehydration-) induced cellular dam- desiccation, rehydration and responses to dehydration age. As we will explain in detail, more recent studies 87 Figure 2. A diagrammatic phylogeny of the major groups of Angiosperms, based on cladistic analysis of the rbcL gene by Chase et al. (1993), summary cladograms in Judd et al. (1999), and information from workshops of the Green Plant Phylogeny Research Coordination Group. A few selected taxa are shown for orientation. Branches without names represent (in some cases large) clades with no known desiccation-tolerant members. Names in bold and with an asterisk indicate all clades with some known desiccation-tolerant members. Parsimony would suggest at least one independent evolution (or re-evolution) of desiccation tolerance in each clade (i.e., at least eight times in the Angiosperms). have corroborated this interpretation and suggested understanding the evolution of vegetative desiccation that vegetative desiccation-tolerant plants can be clas- tolerance. sified into two classes, according to whether their Vegetative desiccation-tolerant plants can be sepa- particular mechanism of tolerance places an emphasis rated into different classes by a third criterion, which upon cellular protection or cellular repair (Oliver & also has importance from an evolutionary standpoint. Bewley 1997). Vegetative desiccation-tolerant plants Some vegetative desiccation-tolerant plants dismantle can also be classified into two groups according to their photosynthetic apparatus and lose their chloro- their sensitivity to rapid water loss. Some vegetative phyll content during desiccation (Tuba et al. 1998). desiccation-tolerant plants can withstand desiccation These plants have been termed poikilochlorophyllous only if it occurs slowly, taking anywhere from 12 h to (Hambler 1961; Gaff 1977, 1989; Bewley 1979). several days to reach the air-dried state. Other plants Desiccation-tolerant plants that retain their photosyn- can survive water loss even if the air-dried state is thetic apparatus in the dried state are termed ho- achieved within an hour. From all that we know so moiochlorophyllous. Plants that require a slow rate of far (see below), it also appears that those vegetative water loss to survive desiccation can be either poikilo- desiccation-tolerant plants that can survive desiccation chlorophyllous or homoiochlorophyllous. All plants even if water loss is